Cited by 1,021Parkinson's Disease Mechanisms and TreatmentsNuclear Receptors and SignalingNeuroinflammation and Neurodegeneration Mechanisms

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Parkinson's disease: a dual‐hit hypothesis

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Hawkes, C. H., Del Tredici, K., Braak, H.·2007·Neuropathology and Applied Neurobiology

DOI 10.1111/j.1365-2990.2007.00874.xPMC PMC7194308

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Abstract

Accumulating evidence suggests that sporadic Parkinson's disease has a long prodromal period during which several non-motor features develop, in particular, impairment of olfaction, vagal dysfunction and sleep disorder. Early sites of Lewy pathology are the olfactory bulb and enteric plexus of the stomach. We propose that a neurotropic pathogen, probably viral, enters the brain via two routes: (i) nasal, with anterograde progression into the temporal lobe; and (ii) gastric, secondary to swallowing of nasal secretions in saliva. These secretions might contain a neurotropic pathogen that, after penetration of the epithelial lining, could enter axons of the Meissner's plexus and, via transsynaptic transmission, reach the preganglionic parasympathetic motor neurones of the vagus nerve. This would allow retrograde transport into the medulla and, from here, into the pons and midbrain until the substantia nigra is reached and typical aspects of disease commence. Evidence for this theory from the perspective of olfactory and autonomic dysfunction is reviewed, and the possible routes of pathogenic invasion are considered. It is concluded that the most parsimonious explanation for the initial events of sporadic Parkinson's disease is pathogenic access to the brain through the stomach and nose - hence the term 'dual-hit'.

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Additional file 1 of Trans-synaptic and retrograde axonal spread of Lewy pathology following pre-formed fibril injection in an in vivo A53T alpha-synuclein mouse model of synucleinopathy
Schaser, A. J., Stackhouse, T. L., Weston, L. J., Kerstein, P. C., Osterberg, V. R., López, C. S., Dickson, D. W., Luk, K. C., Meshul, C. K., Woltjer, R. L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12891207
Additional file 5 of Gut microbiota, circulating cytokines and dementia: a Mendelian randomization study
Ji, D., Chen, W.-Z., Zhang, L., Zhang, Z.-H., & Chen, L.-J. (2024) · Figshare · doi:10.6084/m9.figshare.26660615
Additional file 9 of Gut microbiota, circulating cytokines and dementia: a Mendelian randomization study
Ji, D., Chen, W.-Z., Zhang, L., Zhang, Z.-H., & Chen, L.-J. (2024) · Figshare · doi:10.6084/m9.figshare.26660627
Additional file 13 of Accumulation of alpha-synuclein within the liver, potential role in the clearance of brain pathology associated with Parkinson’s disease
Reyes, J. F., Ekmark‐Lewén, S., Perdiki, Μ., Klingstedt, T., Hoffmann, A., Wiecheć, E., Nilsson, P., Nilsson, K. P. R., Alafuzoff, I., Ingelsson, M., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14253576
Additional file 1 of CSF total and oligomeric α-Synuclein along with TNF-α as risk biomarkers for Parkinson’s disease: a study in LRRK2 mutation carriers
Majbour, N. K., Aasly, J. O., Hustad, E., Thomas, M. A., Vaikath, N. N., Elkum, N., van de Berg, W. D. J., Tokuda, T., Mollenhauer, B., Berendse, H. W., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12262919
Additional file 10 of Trans-synaptic and retrograde axonal spread of Lewy pathology following pre-formed fibril injection in an in vivo A53T alpha-synuclein mouse model of synucleinopathy
Schaser, A. J., Stackhouse, T. L., Weston, L. J., Kerstein, P. C., Osterberg, V. R., López, C. S., Dickson, D. W., Luk, K. C., Meshul, C. K., Woltjer, R. L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12891198
Additional file 1 of Gut microbiota, circulating cytokines and dementia: a Mendelian randomization study
Ji, D., Chen, W.-Z., Zhang, L., Zhang, Z.-H., & Chen, L.-J. (2024) · Figshare · doi:10.6084/m9.figshare.24946444
Additional file 7 of Gut microbiota, circulating cytokines and dementia: a Mendelian randomization study
Ji, D., Chen, W.-Z., Zhang, L., Zhang, Z.-H., & Chen, L.-J. (2024) · Figshare · doi:10.6084/m9.figshare.26660621
Additional file 2 of Gut microbiota, circulating cytokines and dementia: a Mendelian randomization study
Ji, D., Chen, W.-Z., Zhang, L., Zhang, Z.-H., & Chen, L.-J. (2024) · Figshare · doi:10.6084/m9.figshare.24946649
Additional file 5 of Discrimination of MSA-P and MSA-C by RT-QuIC analysis of olfactory mucosa: the first assessment of assay reproducibility between two specialized laboratories
Bargar, C., Luca, C. M. G. D., Devigili, G., Elia, A. E., Cilia, R., Portaleone, S. M., Wang, W., Tramacere, I., Bistaffa, E., Cazzaniga, F. A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17163353
Additional file 4 of Gut microbiota, circulating cytokines and dementia: a Mendelian randomization study
Ji, D., Chen, W.-Z., Zhang, L., Zhang, Z.-H., & Chen, L.-J. (2024) · Figshare · doi:10.6084/m9.figshare.26660612
Additional file 10 of Accumulation of alpha-synuclein within the liver, potential role in the clearance of brain pathology associated with Parkinson’s disease
Reyes, J. F., Ekmark‐Lewén, S., Perdiki, Μ., Klingstedt, T., Hoffmann, A., Wiecheć, E., Nilsson, P., Nilsson, K. P. R., Alafuzoff, I., Ingelsson, M., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14253567
Additional file 2 of Trans-synaptic and retrograde axonal spread of Lewy pathology following pre-formed fibril injection in an in vivo A53T alpha-synuclein mouse model of synucleinopathy
Schaser, A. J., Stackhouse, T. L., Weston, L. J., Kerstein, P. C., Osterberg, V. R., López, C. S., Dickson, D. W., Luk, K. C., Meshul, C. K., Woltjer, R. L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12891210
Additional file 6 of Gut microbiota, circulating cytokines and dementia: a Mendelian randomization study
Ji, D., Chen, W.-Z., Zhang, L., Zhang, Z.-H., & Chen, L.-J. (2024) · Figshare · doi:10.6084/m9.figshare.26660618
Additional file 6 of Trans-synaptic and retrograde axonal spread of Lewy pathology following pre-formed fibril injection in an in vivo A53T alpha-synuclein mouse model of synucleinopathy
Schaser, A. J., Stackhouse, T. L., Weston, L. J., Kerstein, P. C., Osterberg, V. R., López, C. S., Dickson, D. W., Luk, K. C., Meshul, C. K., Woltjer, R. L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12891222
Additional file 4 of Discrimination of MSA-P and MSA-C by RT-QuIC analysis of olfactory mucosa: the first assessment of assay reproducibility between two specialized laboratories
Bargar, C., Luca, C. M. G. D., Devigili, G., Elia, A. E., Cilia, R., Portaleone, S. M., Wang, W., Tramacere, I., Bistaffa, E., Cazzaniga, F. A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17163347
Additional file 3 of Discrimination of MSA-P and MSA-C by RT-QuIC analysis of olfactory mucosa: the first assessment of assay reproducibility between two specialized laboratories
Bargar, C., Luca, C. M. G. D., Devigili, G., Elia, A. E., Cilia, R., Portaleone, S. M., Wang, W., Tramacere, I., Bistaffa, E., Cazzaniga, F. A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17163344
Additional file 12 of Accumulation of alpha-synuclein within the liver, potential role in the clearance of brain pathology associated with Parkinson’s disease
Reyes, J. F., Ekmark‐Lewén, S., Perdiki, Μ., Klingstedt, T., Hoffmann, A., Wiecheć, E., Nilsson, P., Nilsson, K. P. R., Alafuzoff, I. I., Ingelsson, M., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14253573
Additional file 8 of Gut microbiota, circulating cytokines and dementia: a Mendelian randomization study
Ji, D., Chen, W.-Z., Zhang, L., Zhang, Z.-H., & Chen, L.-J. (2024) · Figshare · doi:10.6084/m9.figshare.26660624
Additional file 7 of Trans-synaptic and retrograde axonal spread of Lewy pathology following pre-formed fibril injection in an in vivo A53T alpha-synuclein mouse model of synucleinopathy
Schaser, A. J., Stackhouse, T. L., Weston, L. J., Kerstein, P. C., Osterberg, V. R., López, C. S., Dickson, D. W., Luk, K. C., Meshul, C. K., Woltjer, R. L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12891225
Additional file 3 of Gut microbiota, circulating cytokines and dementia: a Mendelian randomization study
Ji, D., Chen, W.-Z., Zhang, L., Zhang, Z.-H., & Chen, L.-J. (2024) · Figshare · doi:10.6084/m9.figshare.26660609
Additional file 10 of Gut microbiota, circulating cytokines and dementia: a Mendelian randomization study
Ji, D., Chen, W.-Z., Zhang, L., Zhang, Z.-H., & Chen, L.-J. (2024) · Figshare · doi:10.6084/m9.figshare.26660630
Additional file 11 of Accumulation of alpha-synuclein within the liver, potential role in the clearance of brain pathology associated with Parkinson’s disease
Reyes, J. F., Ekmark‐Lewén, S., Perdiki, Μ., Klingstedt, T., Hoffmann, A., Wiecheć, E., Nilsson, P., Nilsson, K. P. R., Alafuzoff, I., Ingelsson, M., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14253570
Additional file 5 of Trans-synaptic and retrograde axonal spread of Lewy pathology following pre-formed fibril injection in an in vivo A53T alpha-synuclein mouse model of synucleinopathy
Schaser, A. J., Stackhouse, T. L., Weston, L. J., Kerstein, P. C., Osterberg, V. R., López, C. S., Dickson, D. W., Luk, K. C., Meshul, C. K., Woltjer, R. L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12891219
Additional file 11 of Trans-synaptic and retrograde axonal spread of Lewy pathology following pre-formed fibril injection in an in vivo A53T alpha-synuclein mouse model of synucleinopathy
Schaser, A. J., Stackhouse, T. L., Weston, L. J., Kerstein, P. C., Osterberg, V. R., López, C. S., Dickson, D. W., Luk, K. C., Meshul, C. K., Woltjer, R. L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12891201
Additional file 3 of Trans-synaptic and retrograde axonal spread of Lewy pathology following pre-formed fibril injection in an in vivo A53T alpha-synuclein mouse model of synucleinopathy
Schaser, A. J., Stackhouse, T. L., Weston, L. J., Kerstein, P. C., Osterberg, V. R., López, C. S., Dickson, D. W., Luk, K. C., Meshul, C. K., Woltjer, R. L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12891213
Additional file 4 of Trans-synaptic and retrograde axonal spread of Lewy pathology following pre-formed fibril injection in an in vivo A53T alpha-synuclein mouse model of synucleinopathy
Schaser, A. J., Stackhouse, T. L., Weston, L. J., Kerstein, P. C., Osterberg, V. R., López, C. S., Dickson, D. W., Luk, K. C., Meshul, C. K., Woltjer, R. L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12891216
Additional file 12 of Trans-synaptic and retrograde axonal spread of Lewy pathology following pre-formed fibril injection in an in vivo A53T alpha-synuclein mouse model of synucleinopathy
Schaser, A. J., Stackhouse, T. L., Weston, L. J., Kerstein, P. C., Osterberg, V. R., López, C. S., Dickson, D. W., Luk, K. C., Meshul, C. K., Woltjer, R. L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12891204
Additional file 1 of Discrimination of MSA-P and MSA-C by RT-QuIC analysis of olfactory mucosa: the first assessment of assay reproducibility between two specialized laboratories
Bargar, C., Luca, C. M. G. D., Devigili, G., Elia, A. E., Cilia, R., Portaleone, S. M., Wang, W., Tramacere, I., Bistaffa, E., Cazzaniga, F. A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17163335
Additional file 9 of Trans-synaptic and retrograde axonal spread of Lewy pathology following pre-formed fibril injection in an in vivo A53T alpha-synuclein mouse model of synucleinopathy
Schaser, A. J., Stackhouse, T. L., Weston, L. J., Kerstein, P. C., Osterberg, V. R., López, C. S., Dickson, D. W., Luk, K. C., Meshul, C. K., Woltjer, R. L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12891231
Additional file 2 of Discrimination of MSA-P and MSA-C by RT-QuIC analysis of olfactory mucosa: the first assessment of assay reproducibility between two specialized laboratories
Bargar, C., Luca, C. M. G. D., Devigili, G., Elia, A. E., Cilia, R., Portaleone, S. M., Wang, W., Tramacere, I., Bistaffa, E., Cazzaniga, F. A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.17163338
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Swathi, N. L., Umar, T. P., Elenien, W. I. A., Bhagat, S., Sakini, A. S. A., & Nand, S. (2025) · Interdisciplinary biotechnological advances · doi:10.1007/978-981-95-2104-3_6
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Khalafi, P., Vogel, J. W., Boghammer, P., Raunio, A., Kivistö, V., Savola, S. E., Kok, E., Mikhailenko, E., Myllykangas, L., & Dagher, A. (2026) · medRxiv · doi:10.64898/2026.01.13.26343943
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Lard, M., deol, S., Dhanawat, M., Gupta, N., Bansal, S., Bhatia, M., Morsy, M. A., Nair, A. B., Krishan, P., Gupta, S., et al. (2026) · Current Nutrition & Food Science · doi:10.2174/0115734013378452251021013702
Spatial transcriptomics reveals the molecular signatures of prodromal and advanced α-synucleinopathy
Lin, L., Jensen, N. M., Ferreira, S. A., Delaidelli, A., Moreira, D. G., Ahlgreen, O. A., Richner, M., Jensen, P. H., Romero‐Ramos, M., Vægter, C. B., et al. (2026) · iScience · doi:10.1016/j.isci.2026.114845
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Yamagchi, A., Ishikawa, K.-I., & Akamatsu, W. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.07.704302
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Kang, S., Na, H. K., Yoon, S. H., Kim, H.-K., Ryu, Y. H., Lee, H. S., Yoo, H. S., & Lyoo, C. H. (2026) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2026.02.007
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Жукова, Н. Г., Sayfitdinkhuzhaev, Z. F., Israilova, G. M., Bustonov, O. Y., Nasriddinova, N. A., Gaponova, O. V., Zhukova, I. A., & Masenko, A. Y. (2026) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-026-01998-x
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Authors: Hawkes, C. H., Del Tredici, K., & Braak, H.
Affiliations: Queen's Hospital (GB)
Goethe University Frankfurt (DE)
Corresponding author: Hawkes, C. H.
ORCID: Hawkes, C. H.
Braak, H.
Venue: Neuropathology and Applied Neurobiology
Publisher: Wiley
Published: 2007-10-24
Volume: 33
Issue: 6
Pages: 599-614
ISSN: 0305-1846 (ISSN-L)
1365-2990
DOI: 10.1111/j.1365-2990.2007.00874.x
PMC: PMC7194308
OpenAlex: W2105047187
Cited by: 1,021
References: 163
Citations by year: 2026: 35 · 2025: 59 · 2024: 87 · 2023: 82 · 2022: 104 · 2021: 117 · 2020: 83 · 2019: 59 · 2018: 49 · 2017: 63 · 2016: 41 · 2015: 33 · 2014: 32 · 2013: 40 · 2012: 33
FWCI: 2.90
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Neuropathology and Applied Neurobiology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Deutsche Forschungsgemeinschaft
Topics: Health Sciences › Medicine › Clinical Neurology › Parkinson's Disease Mechanisms and Treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Receptors and Signaling
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: Parkinson's disease, neurotropic viruses, olfactory dysfunction, Lewy bodies, vagal dysfunction, sleep disorder, olfactory bulb, submucosal plexus, vagus nerve, substantia nigra, prodromal Parkinson's disease, viral pathogenesis
MeSH terms: Animals, Olfaction Disorders, Gastrointestinal Diseases, Heart Diseases, Humans, Models, Neurological, Parkinson Disease, Sleep Wake Disorders, Virus Diseases

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Parkinson's disease: a dual‐hit hypothesis

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